A visual pathway for skylight polarization processing in Drosophila

SUMMARYMany insects use patterns of polarized light in the sky to orient and navigate. Here we functionally characterize neural circuitry in the fruit fly, Drosophila melanogaster, that conveys polarized light signals from the eye to the central complex, a brain region essential for the fly’s sense of direction. Neurons tuned to the angle of polarization of ultraviolet light are found throughout the anterior visual pathway, connecting the optic lobes with the central complex via the anterior optic tubercle and bulb, in a homologous organization to the ‘sky compass’ pathways described in other insects. We detail how a consistent, map-like organization of neural tunings in the peripheral visual system is transformed into a reduced representation suited to flexible processing in the central brain. This study identifies computational motifs of the transformation, enabling mechanistic comparisons of multisensory integration and central processing for navigation in the brains of insects.

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A visual pathway for skylight polarization processing in Drosophila

eLife ◽

10.7554/elife.63225 ◽

2021 ◽

Vol 10 ◽

Author(s):

Ben J Hardcastle ◽

Jaison J Omoto ◽

Pratyush Kandimalla ◽

Bao-Chau M Nguyen ◽

Mehmet F Keleş ◽

...

Keyword(s):

Polarized Light ◽

Fruit Fly ◽

Visual Pathway ◽

Central Complex ◽

Reduced Representation ◽

Central Processing ◽

Use Patterns ◽

Sense Of Direction ◽

Skylight Polarization ◽

Central Brain

Many insects use patterns of polarized light in the sky to orient and navigate. Here we functionally characterize neural circuitry in the fruit fly, Drosophila melanogaster, that conveys polarized light signals from the eye to the central complex, a brain region essential for the fly's sense of direction. Neurons tuned to the angle of polarization of ultraviolet light are found throughout the anterior visual pathway, connecting the optic lobes with the central complex via the anterior optic tubercle and bulb, in a homologous organization to the 'sky compass' pathways described in other insects. We detail how a consistent, map-like organization of neural tunings in the peripheral visual system is transformed into a reduced representation suited to flexible processing in the central brain. This study identifies computational motifs of the transformation, enabling mechanistic comparisons of multisensory integration and central processing for navigation in the brains of insects.

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Synaptic targets of photoreceptors specialized to detect color and skylight polarization in Drosophila

eLife ◽

10.7554/elife.71858 ◽

2021 ◽

Vol 10 ◽

Author(s):

Emil Kind ◽

Kit D Longden ◽

Aljoscha Nern ◽

Arthur Zhao ◽

Gizem Sancer ◽

...

Keyword(s):

Neural Circuits ◽

Polarized Light ◽

Cell Types ◽

Brain Regions ◽

Complementary Information ◽

Color Processing ◽

Optic Lobes ◽

Skylight Polarization ◽

The World ◽

Central Brain

Color and polarization provide complementary information about the world and are detected by specialized photoreceptors. However, the downstream neural circuits that process these distinct modalities are incompletely understood in any animal. Using electron microscopy, we have systematically reconstructed the synaptic targets of the photoreceptors specialized to detect color and skylight polarization in Drosophila, and we have used light microscopy to confirm many of our findings. We identified known and novel downstream targets that are selective for different wavelengths or polarized light, and followed their projections to other areas in the optic lobes and the central brain. Our results revealed many synapses along the photoreceptor axons between brain regions, new pathways in the optic lobes, and spatially segregated projections to central brain regions. Strikingly, photoreceptors in the polarization-sensitive dorsal rim area target fewer cell types, and lack strong connections to the lobula, a neuropil involved in color processing. Our reconstruction identifies shared wiring and modality-specific specializations for color and polarization vision, and provides a comprehensive view of the first steps of the pathways processing color and polarized light inputs.

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A Connectome of the Adult Drosophila Central Brain

10.1101/2020.01.21.911859 ◽

2020 ◽

Cited By ~ 34

Author(s):

C. Shan Xu ◽

Michal Januszewski ◽

Zhiyuan Lu ◽

Shin-ya Takemura ◽

Kenneth J. Hayworth ◽

...

Keyword(s):

Large Fraction ◽

Large Data ◽

Fruit Fly ◽

Cell Types ◽

Brain Regions ◽

Central Complex ◽

Data Set ◽

New Methods ◽

Central Brain ◽

The Brain

AbstractThe neural circuits responsible for behavior remain largely unknown. Previous efforts have reconstructed the complete circuits of small animals, with hundreds of neurons, and selected circuits for larger animals. Here we (the FlyEM project at Janelia and collaborators at Google) summarize new methods and present the complete circuitry of a large fraction of the brain of a much more complex animal, the fruit fly Drosophila melanogaster. Improved methods include new procedures to prepare, image, align, segment, find synapses, and proofread such large data sets; new methods that define cell types based on connectivity in addition to morphology; and new methods to simplify access to a large and evolving data set. From the resulting data we derive a better definition of computational compartments and their connections; an exhaustive atlas of cell examples and types, many of them novel; detailed circuits for most of the central brain; and exploration of the statistics and structure of different brain compartments, and the brain as a whole. We make the data public, with a web site and resources specifically designed to make it easy to explore, for all levels of expertise from the expert to the merely curious. The public availability of these data, and the simplified means to access it, dramatically reduces the effort needed to answer typical circuit questions, such as the identity of upstream and downstream neural partners, the circuitry of brain regions, and to link the neurons defined by our analysis with genetic reagents that can be used to study their functions.Note: In the next few weeks, we will release a series of papers with more involved discussions. One paper will detail the hemibrain reconstruction with more extensive analysis and interpretation made possible by this dense connectome. Another paper will explore the central complex, a brain region involved in navigation, motor control, and sleep. A final paper will present insights from the mushroom body, a center of multimodal associative learning in the fly brain.

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Functional divisions for visual processing in the central brain of flying Drosophila

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1514415112 ◽

2015 ◽

Vol 112 (40) ◽

pp. E5523-E5532 ◽

Cited By ~ 70

Author(s):

Peter T. Weir ◽

Michael H. Dickinson

Keyword(s):

Visual Processing ◽

Visual Stimuli ◽

Automated Analysis ◽

Fruit Fly ◽

Cell Types ◽

Visual Responses ◽

Behavioral Context ◽

Central Brain ◽

Brain Circuit ◽

The Brain

Although anatomy is often the first step in assigning functions to neural structures, it is not always clear whether architecturally distinct regions of the brain correspond to operational units. Whereas neuroarchitecture remains relatively static, functional connectivity may change almost instantaneously according to behavioral context. We imaged panneuronal responses to visual stimuli in a highly conserved central brain region in the fruit fly, Drosophila, during flight. In one substructure, the fan-shaped body, automated analysis revealed three layers that were unresponsive in quiescent flies but became responsive to visual stimuli when the animal was flying. The responses of these regions to a broad suite of visual stimuli suggest that they are involved in the regulation of flight heading. To identify the cell types that underlie these responses, we imaged activity in sets of genetically defined neurons with arborizations in the targeted layers. The responses of this collection during flight also segregated into three sets, confirming the existence of three layers, and they collectively accounted for the panneuronal activity. Our results provide an atlas of flight-gated visual responses in a central brain circuit.

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An unbiased template of the Drosophila brain and ventral nerve cord

PLoS ONE ◽

10.1371/journal.pone.0236495 ◽

2020 ◽

Vol 15 (12) ◽

pp. e0236495

Author(s):

John A. Bogovic ◽

Hideo Otsuna ◽

Larissa Heinrich ◽

Masayoshi Ito ◽

Jennifer Jeter ◽

...

Keyword(s):

Nerve Cord ◽

Ventral Nerve Cord ◽

Model Organism ◽

Fruit Fly ◽

Tissue Preparation ◽

Best Available Technologies ◽

Common Reference ◽

Biological Studies ◽

Reference Space ◽

Central Brain

The fruit fly Drosophila melanogaster is an important model organism for neuroscience with a wide array of genetic tools that enable the mapping of individual neurons and neural subtypes. Brain templates are essential for comparative biological studies because they enable analyzing many individuals in a common reference space. Several central brain templates exist for Drosophila, but every one is either biased, uses sub-optimal tissue preparation, is imaged at low resolution, or does not account for artifacts. No publicly available Drosophila ventral nerve cord template currently exists. In this work, we created high-resolution templates of the Drosophila brain and ventral nerve cord using the best-available technologies for imaging, artifact correction, stitching, and template construction using groupwise registration. We evaluated our central brain template against the four most competitive, publicly available brain templates and demonstrate that ours enables more accurate registration with fewer local deformations in shorter time.

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Parallel visual pathways with topographic versus non-topographic organization connect the Drosophila eyes to the central brain

10.1101/2020.04.11.037333 ◽

2020 ◽

Cited By ~ 2

Author(s):

Lorin Timaeus ◽

Laura Geid ◽

Gizem Sancer ◽

Mathias F. Wernet ◽

Thomas Hummel

Keyword(s):

Visual Information ◽

Visual Cues ◽

Spatial Information ◽

Central Complex ◽

Structural Basis ◽

Projection Neurons ◽

Central Brain ◽

Retinotopic Organization ◽

Dendritic Fields ◽

Parallel Visual Pathways

SummaryOne hallmark of the visual system is the strict retinotopic organization from the periphery towards the central brain, spanning multiple layers of synaptic integration. Recent Drosophila studies on the computation of distinct visual features have shown that retinotopic representation is often lost beyond the optic lobes, due to convergence of columnar neuron types onto optic glomeruli. Nevertheless, functional imaging revealed a spatially accurate representation of visual cues in the central complex (CX), raising the question how this is implemented on a circuit level. By characterizing the afferents to a specific visual glomerulus, the anterior optic tubercle (AOTU), we discovered a spatial segregation of topographic versus non-topographic projections from molecularly distinct classes of medulla projection neurons (medullo-tubercular, or MeTu neurons). Distinct classes of topographic versus non-topographic MeTus form parallel channels, terminating in separate AOTU domains. Both types then synapse onto separate matching topographic fields of tubercular-bulbar (TuBu) neurons which relay visual information towards the dendritic fields of central complex ring neurons in the bulb neuropil, where distinct bulb sectors correspond to a distinct ring domain in the ellipsoid body. Hence, peripheral topography is maintained due to stereotypic circuitry within each TuBu class, providing the structural basis for spatial representation of visual information in the central complex. Together with previous data showing rough topography of lobula projections to a different AOTU subunit, our results further highlight the AOTUs role as a prominent relay station for spatial information from the retina to the central brain.

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Homothorax controls a binary Rhodopsin switch in Drosophila ocelli

PLoS Genetics ◽

10.1371/journal.pgen.1009460 ◽

2021 ◽

Vol 17 (7) ◽

pp. e1009460

Author(s):

Abhishek Kumar Mishra ◽

Cornelia Fritsch ◽

Roumen Voutev ◽

Richard S. Mann ◽

Simon G. Sprecher

Keyword(s):

Drosophila Melanogaster ◽

Visual Perception ◽

Compound Eye ◽

Polarized Light ◽

Fruit Fly ◽

Compound Eyes ◽

Ancestral Gene ◽

Evolutionary Diversification ◽

Opsin Genes ◽

A Cell

Visual perception of the environment is mediated by specialized photoreceptor (PR) neurons of the eye. Each PR expresses photosensitive opsins, which are activated by a particular wavelength of light. In most insects, the visual system comprises a pair of compound eyes that are mainly associated with motion, color or polarized light detection, and a triplet of ocelli that are thought to be critical during flight to detect horizon and movements. It is widely believed that the evolutionary diversification of compound eye and ocelli in insects occurred from an ancestral visual organ around 500 million years ago. Concurrently, opsin genes were also duplicated to provide distinct spectral sensitivities to different PRs of compound eye and ocelli. In the fruit fly Drosophila melanogaster, Rhodopsin1 (Rh1) and Rh2 are closely related opsins that originated from the duplication of a single ancestral gene. However, in the visual organs, Rh2 is uniquely expressed in ocelli whereas Rh1 is uniquely expressed in outer PRs of the compound eye. It is currently unknown how this differential expression of Rh1 and Rh2 in the two visual organs is controlled to provide unique spectral sensitivities to ocelli and compound eyes. Here, we show that Homothorax (Hth) is expressed in ocelli and confers proper rhodopsin expression. We find that Hth controls a binary Rhodopsin switch in ocelli to promote Rh2 expression and repress Rh1 expression. Genetic and molecular analysis of rh1 and rh2 supports that Hth acts through their promoters to regulate Rhodopsin expression in the ocelli. Finally, we also show that when ectopically expressed in the retina, hth is sufficient to induce Rh2 expression only at the outer PRs in a cell autonomous manner. We therefore propose that the diversification of rhodpsins in the ocelli and retinal outer PRs occurred by duplication of an ancestral gene, which is under the control of Homothorax.

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The head direction circuit of two insect species

10.1101/854521 ◽

2019 ◽

Cited By ~ 1

Author(s):

Ioannis Pisokas ◽

Stanley Heinze ◽

Barbara Webb

Keyword(s):

Fruit Fly ◽

Central Complex ◽

Insect Species ◽

Comparative Approach ◽

Head Direction ◽

Circuit Performance ◽

Heading Direction ◽

Neuronal Projection ◽

Connectivity Patterns ◽

The Brain

AbstractRecent studies of the Central Complex in the brain of the fruit fly have identified neurons with activity that tracks the animal’s heading direction. These neurons are part of a neuronal circuit with dynamics resembling those of a ring attractor. Other insects have a homologous circuit sharing a generally similar topographic structure but with significant structural and connectivity differences. We model the connectivity patterns in two insect species to investigate the effect of the differences on the dynamics of the circuit. We illustrate that the circuit found in locusts can also operate as a ring attractor and identify differences that enable the fruit fly circuit to respond faster to heading changes while they render the locust circuit more tolerant to noise. Our findings demonstrate that subtle differences in neuronal projection patterns can have a significant effect on the circuit performance and emphasise the need for a comparative approach in neuroscience.

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Polarized Skylight Navigation in Insects: Model and Electrophysiology of e-Vector Coding by Neurons in the Central Complex

Journal of Neurophysiology ◽

10.1152/jn.00784.2007 ◽

2008 ◽

Vol 99 (2) ◽

pp. 667-682 ◽

Cited By ~ 62

Author(s):

Midori Sakura ◽

Dimitrios Lambrinos ◽

Thomas Labhart

Keyword(s):

Vision System ◽

Gain Control ◽

Central Complex ◽

Degree Of Polarization ◽

Insect Brain ◽

Atmospheric Conditions ◽

Compass Orientation ◽

Vector Coding ◽

Skylight Polarization ◽

Vector Orientation

Many insects exploit skylight polarization for visual compass orientation or course control. As found in crickets, the peripheral visual system (optic lobe) contains three types of polarization-sensitive neurons (POL neurons), which are tuned to different (∼60° diverging) e-vector orientations. Thus each e-vector orientation elicits a specific combination of activities among the POL neurons coding any e-vector orientation by just three neural signals. In this study, we hypothesize that in the presumed orientation center of the brain (central complex) e-vector orientation is population-coded by a set of “compass neurons.” Using computer modeling, we present a neural network model transforming the signal triplet provided by the POL neurons to compass neuron activities coding e-vector orientation by a population code. Using intracellular electrophysiology and cell marking, we present evidence that neurons with the response profile of the presumed compass neurons do indeed exist in the insect brain: each of these compass neuron-like (CNL) cells is activated by a specific e-vector orientation only and otherwise remains silent. Morphologically, CNL cells are tangential neurons extending from the lateral accessory lobe to the lower division of the central body. Surpassing the modeled compass neurons in performance, CNL cells are insensitive to the degree of polarization of the stimulus between 99% and at least down to 18% polarization and thus largely disregard variations of skylight polarization due to changing solar elevations or atmospheric conditions. This suggests that the polarization vision system includes a gain control circuit keeping the output activity at a constant level.

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Matched-filter coding of sky polarization results in an internal sun compass in the brain of the desert locust

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2005192117 ◽

2020 ◽

Vol 117 (41) ◽

pp. 25810-25817

Author(s):

Frederick Zittrell ◽

Keram Pfeiffer ◽

Uwe Homberg

Keyword(s):

Spatial Orientation ◽

Matched Filter ◽

Polarized Light ◽

Central Complex ◽

Insect Brain ◽

The Sun ◽

Polarization Pattern ◽

Sun Compass ◽

Small Spot ◽

Polarization Compass

Many animals use celestial cues for spatial orientation. These include the sun and, in insects, the polarization pattern of the sky, which depends on the position of the sun. The central complex in the insect brain plays a key role in spatial orientation. In desert locusts, the angle of polarized light in the zenith above the animal and the direction of a simulated sun are represented in a compass-like fashion in the central complex, but how both compasses fit together for a unified representation of external space remained unclear. To address this question, we analyzed the sensitivity of intracellularly recorded central-complex neurons to the angle of polarized light presented from up to 33 positions in the animal’s dorsal visual field and injected Neurobiotin tracer for cell identification. Neurons were polarization sensitive in large parts of the virtual sky that in some cells extended to the horizon in all directions. Neurons, moreover, were tuned to spatial patterns of polarization angles that matched the sky polarization pattern of particular sun positions. The horizontal components of these calculated solar positions were topographically encoded in the protocerebral bridge of the central complex covering 360° of space. This whole-sky polarization compass does not support the earlier reported polarization compass based on stimulation from a small spot above the animal but coincides well with the previously demonstrated direct sun compass based on unpolarized light stimulation. Therefore, direct sunlight and whole-sky polarization complement each other for robust head direction coding in the locust central complex.

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